An official website of the United States government
Abstract Background Disentangling the drivers of genetic differentiation is one of the cornerstones in evolution. This is because genetic diversity, and the way in which it is partitioned within and among populations across space, is an important asset for the ability of populations to adapt and persist in changing environments. We tested three major hypotheses accounting for genetic differentiation—isolation-by-distance (IBD), isolation-by-environment (IBE) and isolation-by-resistance (IBR)—in the annual plant Arabidopsis thaliana across the Iberian Peninsula, the region with the largest genomic diversity. To that end, we sampled, genotyped with genome-wide SNPs, and analyzed 1772 individuals from 278 populations distributed across the Iberian Peninsula. Results IBD, and to a lesser extent IBE, were the most important drivers of genetic differentiation in A. thaliana . In other words, dispersal limitation, genetic drift, and to a lesser extent local adaptation to environmental gradients, accounted for the within- and among-population distribution of genetic diversity. Analyses applied to the four Iberian genetic clusters, which represent the joint outcome of the long demographic and adaptive history of the species in the region, showed similar results except for one cluster, in which IBR (a function of landscape heterogeneity) was the most important driver of genetic differentiation. Using spatial hierarchical Bayesian models, we found that precipitation seasonality and topsoil pH chiefly accounted for the geographic distribution of genetic diversity in Iberian A. thaliana . Conclusions Overall, the interplay between the influence of precipitation seasonality on genetic diversity and the effect of restricted dispersal and genetic drift on genetic differentiation emerges as the major forces underlying the evolutionary trajectory of Iberian A. thaliana .
more »
« less
Type and intensity of surrounding human land use, not local environment, shape genetic structure of a native grassland plant
Abstract Landscape heterogeneity can shape genetic structure and functional connectivity of populations. When this heterogeneity imposes variable costs of moving across the landscape, populations can be structured according to a pattern of “isolation by resistance” (IBR). At the same time, divergent local environmental filters can limit gene flow, creating an alternative pattern of “isolation by environment” (IBE). Here, we evaluate IBR and IBE in the insect‐pollinated, biennial plantSabatia angularis(L.) Pursh (Gentianaceae) across serpentine grasslands in the fragmented landscape of SE Pennsylvania, USA using ~4500 neutral SNP loci. Specifically, we test the extent to which radical alteration of the landscape matrix by humans has fundamentally altered the cost of movement, imprinting a pattern of IBR dictated by land use type and intensity, and the potential for IBE in relation to a gradient of heavy metal concentrations found in serpentine soil. We reveal a strong signal of IBR and a weak signal of IBE across sites, indicating the greater importance of the landscape matrix in shaping genetic structure ofS. angularispopulations in the study region. Based on Circuitscape and least cost path approaches, we find that both low‐ and high‐intensity urbanization resist gene flow by orders of magnitude greater than “natural” habitats, although resistance to low‐intensity urbanization weakens at larger spatial scales. While cropland presents a substantially lower barrier than urban development, cumulative human land use surrounding populations predicts within‐population genetic diversity and inbreeding inS. angularis. Our results emphasize the role of forest buffers and corridors in facilitating gene flow between serpentine grassland patches and averting local extinction of plant populations.
more »
« less
- Award ID(s):
- 1655772
- PAR ID:
- 10404978
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 30
- Issue:
- 3
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 639-655
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest‐dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation‐by‐distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.more » « less
-
Abstract Understanding the processes that underlie the development of population genetic structure is central to the study of evolution. Patterns of genetic structure, in turn, can reveal signatures of isolation by distance (IBD), barriers to gene flow, or even the genesis of speciation. However, it is unclear how severe range restriction might impact the processes that dominate the development of genetic structure. In narrow endemic species, is population structure likely to be adaptive in nature, or rather the result of genetic drift? In this study, we investigated patterns of genetic diversity and structure in the narrow endemic Hayden's ringlet butterfly. Specifically, we asked to what degree genetic structure in the Hayden's ringlet can be explained by IBD, isolation by resistance (IBR) (in the form of geographic or ecological barriers to migration between populations), and isolation by environment (in the form of differences in host plant availability and preference). We employed a genotyping‐by‐sequencing (GBS) approach coupled with host preference assays, Bayesian modelling, and population genomic analyses to answer these questions. Our results suggest that despite their restricted range, levels of genetic diversity in the Hayden's ringlet are comparable to those seen in more widespread butterfly species. Hayden's ringlets showed a strong preference for feeding on grasses relative to sedges, but neither larval preference nor potential host availability at sampling sites correlated with genetic structure. We conclude that geography, in the form of IBR and simple IBD, was the major driver of contemporary patterns of differentiation in this narrow endemic species.more » « less
-
Abstract Isolation by environment (IBE) is a population genomic pattern that arises when ecological barriers reduce gene flow between populations. Although current evidence suggests IBE is common in nature, few studies have evaluated the underlying mechanisms that generate IBE patterns. In this study, we evaluate five proposed mechanisms of IBE (natural selection against immigrants, sexual selection against immigrants, selection against hybrids, biased dispersal, environment-based phenological differences) that may give rise to host-associated differentiation within a sympatric population of the redheaded pine sawfly, Neodiprion lecontei, a species for which IBE has previously been detected. We first characterize the three pine species used by N. lecontei at the site, finding morphological and chemical differences among the hosts that could generate divergent selection on sawfly host-use traits. Next, using morphometrics and ddRAD sequencing, we detect modest phenotypic and genetic differentiation among sawflies originating from different pines that is consistent with recent, in situ divergence. Finally, via a series of laboratory assays – including assessments of larval performance on different hosts, adult mate and host preferences, hybrid fitness, and adult eclosion timing – we find evidence that multiple mechanisms contribute to IBE in N. lecontei. Overall, our results suggest IBE can emerge quickly, possibly due to multiple mechanisms acting in concert to reduce migration between different environments.more » « less
-
Abstract One key research goal of evolutionary biology is to understand the origin and maintenance of genetic variation. In the Cerrado, the South American savanna located primarily in the Central Brazilian Plateau, many hypotheses have been proposed to explain how landscape features (e.g., geographic distance, river barriers, topographic compartmentalization, and historical climatic fluctuations) have promoted genetic structure by mediating gene flow. Here, we asked whether these landscape features have influenced the genetic structure and differentiation in the lizard speciesNorops brasiliensis(Squamata: Dactyloidae). To achieve our goal, we used a genetic clustering analysis and estimate an effective migration surface to assess genetic structure in the focal species. Optimized isolation-by-resistance models and a simulation-based approach combined with machine learning (convolutional neural network; CNN) were then used to infer current and historical effects on population genetic structure through 12 unique landscape models. We recovered five geographically distributed populations that are separated by regions of lower-than-expected gene flow. The results of the CNN showed that geographic distance is the sole predictor of genetic variation inN. brasiliensis, and that slope, rivers, and historical climate had no discernible influence on gene flow. Our novel CNN approach was accurate (89.5%) in differentiating each landscape model. CNN and other machine learning approaches are still largely unexplored in landscape genetics studies, representing promising avenues for future research with increasingly accessible genomic datasets.more » « less
